Investigation of associations between retinal microvascular parameters and albuminuria in UK Biobank: a cross-sectional case-control study

UK Biobank Eye and Vision Consortium; Euan N. Paterson; Chris Cardwell; Thomas J. MacGillivray; Emanuele Trucco; Alexander S. Doney; Paul Foster; Alexander P. Maxwell; Gareth J. McKay; Tariq Aslam; Sarah Barman; Jenny Barrett; Paul Bishop; Peter Blows; Catey Bunce; Roxana Carare; Usha Chakravarthy; Michelle Chan; Antonietta Chianca; Valentina Cipriani; David Crabb; Philippa Cumberland; Alexander Day; Parul Desai; Bal Dhillon; Andrew Dick; Cathy Egan; Sarah Ennis; Marcus Fruttiger; John Gallacher; David (Ted) Garway-Heath; Jane Gibson; Dan Gore; Jeremy Guggenheim; Chris Hammond; Alison Hardcastle; Simon Harding; Ruth Hogg; Pirro Hysi; Pearse A. Keane; Sir Peng Tee Khaw; Anthony Khawaja; Gerassimos Lascaratos; Andrew Lotery; Phil Luthert; Tom MacGillivray; Sarah Mackie; Keith Martin; Bernadette McGuinness; Gareth McKay; Robyn Tapp

doi:10.1186/s12882-021-02273-6

Investigation of associations between retinal microvascular parameters and albuminuria in UK Biobank: a cross-sectional case-control study

UK Biobank Eye and Vision Consortium, Euan N. Paterson, Chris Cardwell, Thomas J. MacGillivray, Emanuele Trucco, Alexander S. Doney, Paul Foster, Alexander P. Maxwell, Gareth J. McKay, Tariq Aslam, Sarah Barman, Jenny Barrett, Paul Bishop, Peter Blows, Catey Bunce, Roxana Carare, Usha Chakravarthy, Michelle Chan, Antonietta Chianca, Valentina CiprianiDavid Crabb, Philippa Cumberland, Alexander Day, Parul Desai, Bal Dhillon, Andrew Dick, Cathy Egan, Sarah Ennis, Marcus Fruttiger, John Gallacher, David (Ted) Garway-Heath, Jane Gibson, Dan Gore, Jeremy Guggenheim, Chris Hammond, Alison Hardcastle, Simon Harding, Ruth Hogg, Pirro Hysi, Pearse A. Keane, Sir Peng Tee Khaw, Anthony Khawaja, Gerassimos Lascaratos, Andrew Lotery, Phil Luthert, Tom MacGillivray, Sarah Mackie, Keith Martin, Bernadette McGuinness, Gareth McKay, Robyn Tapp

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Abstract

Background: Associations between microvascular variation and chronic kidney disease (CKD) have been reported previously. Non-invasive retinal fundus imaging enables evaluation of the microvascular network and may offer insight to systemic risk associated with CKD. Methods: Retinal microvascular parameters (fractal dimension [FD] – a measure of the complexity of the vascular network, tortuosity, and retinal arteriolar and venular calibre) were quantified from macula-centred fundus images using the Vessel Assessment and Measurement Platform for Images of the REtina (VAMPIRE) version 3.1 (VAMPIRE group, Universities of Dundee and Edinburgh, Scotland) and assessed for associations with renal damage in a case-control study nested within the multi-centre UK Biobank cohort study. Participants were designated cases or controls based on urinary albumin to creatinine ratio (ACR) thresholds. Participants with ACR ≥ 3 mg/mmol (ACR stages A2-A3) were characterised as cases, and those with an ACR < 3 mg/mmol (ACR stage A1) were categorised as controls. Participants were matched on age, sex and ethnic background. Results: Lower FD (less extensive microvascular branching) was associated with a small increase in odds of albuminuria independent of blood pressure, diabetes and other potential confounding variables (odds ratio [OR] 1.18, 95% confidence interval [CI] 1.03–1.34 for arterioles and OR 1.24, CI 1.05–1.47 for venules). Measures of tortuosity or retinal arteriolar and venular calibre were not significantly associated with ACR. Conclusions: This study supports previously reported associations between retinal microvascular FD and other metabolic disturbances affecting the systemic vasculature. The association between retinal microvascular FD and albuminuria, independent of diabetes and blood pressure, may represent a useful indicator of systemic vascular damage associated with albuminuria.

Original language	English
Article number	72
Number of pages	11
Journal	BMC Nephrology
Volume	22
Issue number	1
Early online date	25 Feb 2021
DOIs	https://doi.org/10.1186/s12882-021-02273-6
Publication status	E-pub ahead of print - 25 Feb 2021

Bibliographical note

This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

Funder

This study was supported by funding from the Northern Ireland Kidney Research Fund. The funding body played no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

ASJC Scopus subject areas

Nephrology

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This output contributes to the following UN Sustainable Development Goals (SDGs)

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UK Biobank Eye and Vision Consortium, Paterson, E. N., Cardwell, C., MacGillivray, T. J., Trucco, E., Doney, A. S., Foster, P., Maxwell, A. P., McKay, G. J., Aslam, T., Barman, S., Barrett, J., Bishop, P., Blows, P., Bunce, C., Carare, R., Chakravarthy, U., Chan, M., Chianca, A., ... Tapp, R. (2021). Investigation of associations between retinal microvascular parameters and albuminuria in UK Biobank: a cross-sectional case-control study. BMC Nephrology, 22(1), [72]. https://doi.org/10.1186/s12882-021-02273-6

Investigation of associations between retinal microvascular parameters and albuminuria in UK Biobank : a cross-sectional case-control study. / UK Biobank Eye and Vision Consortium; Paterson, Euan N.; Cardwell, Chris; MacGillivray, Thomas J.; Trucco, Emanuele; Doney, Alexander S.; Foster, Paul; Maxwell, Alexander P.; McKay, Gareth J.; Aslam, Tariq; Barman, Sarah; Barrett, Jenny; Bishop, Paul; Blows, Peter; Bunce, Catey; Carare, Roxana; Chakravarthy, Usha; Chan, Michelle; Chianca, Antonietta; Cipriani, Valentina; Crabb, David; Cumberland, Philippa; Day, Alexander; Desai, Parul; Dhillon, Bal; Dick, Andrew; Egan, Cathy; Ennis, Sarah; Fruttiger, Marcus; Gallacher, John; Garway-Heath, David (Ted); Gibson, Jane; Gore, Dan; Guggenheim, Jeremy; Hammond, Chris; Hardcastle, Alison; Harding, Simon; Hogg, Ruth; Hysi, Pirro; Keane, Pearse A.; Khaw, Sir Peng Tee; Khawaja, Anthony; Lascaratos, Gerassimos; Lotery, Andrew; Luthert, Phil; MacGillivray, Tom; Mackie, Sarah; Martin, Keith; McGuinness, Bernadette; McKay, Gareth; Tapp, Robyn.

In: BMC Nephrology, Vol. 22, No. 1, 72, 25.02.2021.

Research output: Contribution to journal › Article › peer-review

UK Biobank Eye and Vision Consortium, Paterson, EN, Cardwell, C, MacGillivray, TJ, Trucco, E, Doney, AS, Foster, P, Maxwell, AP, McKay, GJ, Aslam, T, Barman, S, Barrett, J, Bishop, P, Blows, P, Bunce, C, Carare, R, Chakravarthy, U, Chan, M, Chianca, A, Cipriani, V, Crabb, D, Cumberland, P, Day, A, Desai, P, Dhillon, B, Dick, A, Egan, C, Ennis, S, Fruttiger, M, Gallacher, J, Garway-Heath, D, Gibson, J, Gore, D, Guggenheim, J, Hammond, C, Hardcastle, A, Harding, S, Hogg, R, Hysi, P, Keane, PA, Khaw, SPT, Khawaja, A, Lascaratos, G, Lotery, A, Luthert, P, MacGillivray, T, Mackie, S, Martin, K, McGuinness, B, McKay, G & Tapp, R 2021, 'Investigation of associations between retinal microvascular parameters and albuminuria in UK Biobank: a cross-sectional case-control study', BMC Nephrology, vol. 22, no. 1, 72. https://doi.org/10.1186/s12882-021-02273-6

UK Biobank Eye and Vision Consortium ; Paterson, Euan N. ; Cardwell, Chris ; MacGillivray, Thomas J. ; Trucco, Emanuele ; Doney, Alexander S. ; Foster, Paul ; Maxwell, Alexander P. ; McKay, Gareth J. ; Aslam, Tariq ; Barman, Sarah ; Barrett, Jenny ; Bishop, Paul ; Blows, Peter ; Bunce, Catey ; Carare, Roxana ; Chakravarthy, Usha ; Chan, Michelle ; Chianca, Antonietta ; Cipriani, Valentina ; Crabb, David ; Cumberland, Philippa ; Day, Alexander ; Desai, Parul ; Dhillon, Bal ; Dick, Andrew ; Egan, Cathy ; Ennis, Sarah ; Fruttiger, Marcus ; Gallacher, John ; Garway-Heath, David (Ted) ; Gibson, Jane ; Gore, Dan ; Guggenheim, Jeremy ; Hammond, Chris ; Hardcastle, Alison ; Harding, Simon ; Hogg, Ruth ; Hysi, Pirro ; Keane, Pearse A. ; Khaw, Sir Peng Tee ; Khawaja, Anthony ; Lascaratos, Gerassimos ; Lotery, Andrew ; Luthert, Phil ; MacGillivray, Tom ; Mackie, Sarah ; Martin, Keith ; McGuinness, Bernadette ; McKay, Gareth ; Tapp, Robyn. / Investigation of associations between retinal microvascular parameters and albuminuria in UK Biobank : a cross-sectional case-control study. In: BMC Nephrology. 2021 ; Vol. 22, No. 1.

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abstract = "Background: Associations between microvascular variation and chronic kidney disease (CKD) have been reported previously. Non-invasive retinal fundus imaging enables evaluation of the microvascular network and may offer insight to systemic risk associated with CKD. Methods: Retinal microvascular parameters (fractal dimension [FD] – a measure of the complexity of the vascular network, tortuosity, and retinal arteriolar and venular calibre) were quantified from macula-centred fundus images using the Vessel Assessment and Measurement Platform for Images of the REtina (VAMPIRE) version 3.1 (VAMPIRE group, Universities of Dundee and Edinburgh, Scotland) and assessed for associations with renal damage in a case-control study nested within the multi-centre UK Biobank cohort study. Participants were designated cases or controls based on urinary albumin to creatinine ratio (ACR) thresholds. Participants with ACR ≥ 3 mg/mmol (ACR stages A2-A3) were characterised as cases, and those with an ACR < 3 mg/mmol (ACR stage A1) were categorised as controls. Participants were matched on age, sex and ethnic background. Results: Lower FD (less extensive microvascular branching) was associated with a small increase in odds of albuminuria independent of blood pressure, diabetes and other potential confounding variables (odds ratio [OR] 1.18, 95% confidence interval [CI] 1.03–1.34 for arterioles and OR 1.24, CI 1.05–1.47 for venules). Measures of tortuosity or retinal arteriolar and venular calibre were not significantly associated with ACR. Conclusions: This study supports previously reported associations between retinal microvascular FD and other metabolic disturbances affecting the systemic vasculature. The association between retinal microvascular FD and albuminuria, independent of diabetes and blood pressure, may represent a useful indicator of systemic vascular damage associated with albuminuria.",

author = "{UK Biobank Eye and Vision Consortium} and Paterson, {Euan N.} and Chris Cardwell and MacGillivray, {Thomas J.} and Emanuele Trucco and Doney, {Alexander S.} and Paul Foster and Maxwell, {Alexander P.} and McKay, {Gareth J.} and Tariq Aslam and Sarah Barman and Jenny Barrett and Paul Bishop and Peter Blows and Catey Bunce and Roxana Carare and Usha Chakravarthy and Michelle Chan and Antonietta Chianca and Valentina Cipriani and David Crabb and Philippa Cumberland and Alexander Day and Parul Desai and Bal Dhillon and Andrew Dick and Cathy Egan and Sarah Ennis and Marcus Fruttiger and John Gallacher and Garway-Heath, {David (Ted)} and Jane Gibson and Dan Gore and Jeremy Guggenheim and Chris Hammond and Alison Hardcastle and Simon Harding and Ruth Hogg and Pirro Hysi and Keane, {Pearse A.} and Khaw, {Sir Peng Tee} and Anthony Khawaja and Gerassimos Lascaratos and Andrew Lotery and Phil Luthert and Tom MacGillivray and Sarah Mackie and Keith Martin and Bernadette McGuinness and Gareth McKay and Robyn Tapp",

note = "This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.",

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month = feb,

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doi = "10.1186/s12882-021-02273-6",

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T1 - Investigation of associations between retinal microvascular parameters and albuminuria in UK Biobank

T2 - a cross-sectional case-control study

AU - UK Biobank Eye and Vision Consortium

AU - Paterson, Euan N.

AU - Cardwell, Chris

AU - MacGillivray, Thomas J.

AU - Trucco, Emanuele

AU - Doney, Alexander S.

AU - Foster, Paul

AU - Maxwell, Alexander P.

AU - McKay, Gareth J.

AU - Aslam, Tariq

AU - Barman, Sarah

AU - Barrett, Jenny

AU - Bishop, Paul

AU - Blows, Peter

AU - Bunce, Catey

AU - Carare, Roxana

AU - Chakravarthy, Usha

AU - Chan, Michelle

AU - Chianca, Antonietta

AU - Cipriani, Valentina

AU - Crabb, David

AU - Cumberland, Philippa

AU - Day, Alexander

AU - Desai, Parul

AU - Dhillon, Bal

AU - Dick, Andrew

AU - Egan, Cathy

AU - Ennis, Sarah

AU - Fruttiger, Marcus

AU - Gallacher, John

AU - Garway-Heath, David (Ted)

AU - Gibson, Jane

AU - Gore, Dan

AU - Guggenheim, Jeremy

AU - Hammond, Chris

AU - Hardcastle, Alison

AU - Harding, Simon

AU - Hogg, Ruth

AU - Hysi, Pirro

AU - Keane, Pearse A.

AU - Khaw, Sir Peng Tee

AU - Khawaja, Anthony

AU - Lascaratos, Gerassimos

AU - Lotery, Andrew

AU - Luthert, Phil

AU - MacGillivray, Tom

AU - Mackie, Sarah

AU - Martin, Keith

AU - McGuinness, Bernadette

AU - McKay, Gareth

AU - Tapp, Robyn

N1 - This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.

PY - 2021/2/25

Y1 - 2021/2/25

N2 - Background: Associations between microvascular variation and chronic kidney disease (CKD) have been reported previously. Non-invasive retinal fundus imaging enables evaluation of the microvascular network and may offer insight to systemic risk associated with CKD. Methods: Retinal microvascular parameters (fractal dimension [FD] – a measure of the complexity of the vascular network, tortuosity, and retinal arteriolar and venular calibre) were quantified from macula-centred fundus images using the Vessel Assessment and Measurement Platform for Images of the REtina (VAMPIRE) version 3.1 (VAMPIRE group, Universities of Dundee and Edinburgh, Scotland) and assessed for associations with renal damage in a case-control study nested within the multi-centre UK Biobank cohort study. Participants were designated cases or controls based on urinary albumin to creatinine ratio (ACR) thresholds. Participants with ACR ≥ 3 mg/mmol (ACR stages A2-A3) were characterised as cases, and those with an ACR < 3 mg/mmol (ACR stage A1) were categorised as controls. Participants were matched on age, sex and ethnic background. Results: Lower FD (less extensive microvascular branching) was associated with a small increase in odds of albuminuria independent of blood pressure, diabetes and other potential confounding variables (odds ratio [OR] 1.18, 95% confidence interval [CI] 1.03–1.34 for arterioles and OR 1.24, CI 1.05–1.47 for venules). Measures of tortuosity or retinal arteriolar and venular calibre were not significantly associated with ACR. Conclusions: This study supports previously reported associations between retinal microvascular FD and other metabolic disturbances affecting the systemic vasculature. The association between retinal microvascular FD and albuminuria, independent of diabetes and blood pressure, may represent a useful indicator of systemic vascular damage associated with albuminuria.

AB - Background: Associations between microvascular variation and chronic kidney disease (CKD) have been reported previously. Non-invasive retinal fundus imaging enables evaluation of the microvascular network and may offer insight to systemic risk associated with CKD. Methods: Retinal microvascular parameters (fractal dimension [FD] – a measure of the complexity of the vascular network, tortuosity, and retinal arteriolar and venular calibre) were quantified from macula-centred fundus images using the Vessel Assessment and Measurement Platform for Images of the REtina (VAMPIRE) version 3.1 (VAMPIRE group, Universities of Dundee and Edinburgh, Scotland) and assessed for associations with renal damage in a case-control study nested within the multi-centre UK Biobank cohort study. Participants were designated cases or controls based on urinary albumin to creatinine ratio (ACR) thresholds. Participants with ACR ≥ 3 mg/mmol (ACR stages A2-A3) were characterised as cases, and those with an ACR < 3 mg/mmol (ACR stage A1) were categorised as controls. Participants were matched on age, sex and ethnic background. Results: Lower FD (less extensive microvascular branching) was associated with a small increase in odds of albuminuria independent of blood pressure, diabetes and other potential confounding variables (odds ratio [OR] 1.18, 95% confidence interval [CI] 1.03–1.34 for arterioles and OR 1.24, CI 1.05–1.47 for venules). Measures of tortuosity or retinal arteriolar and venular calibre were not significantly associated with ACR. Conclusions: This study supports previously reported associations between retinal microvascular FD and other metabolic disturbances affecting the systemic vasculature. The association between retinal microvascular FD and albuminuria, independent of diabetes and blood pressure, may represent a useful indicator of systemic vascular damage associated with albuminuria.

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Investigation of associations between retinal microvascular parameters and albuminuria in UK Biobank: a cross-sectional case-control study

Abstract

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UN SDGs

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